Induction of microrna-21 with exogenous hydrogen sulfide attenuates myocardial ischemic and inflammatory injury in mice

Circulation: Cardiovascular Genetics

Volumn 7, Issue 3, 2014, Pages 311-320

  Toldo, Stefano ^a   Das, Anindita ^a   Mezzaroma, Eleonora ^a   Chau, Vinh Q ^a   Marchetti, Carlo ^a   Durrant, David ^a   Samidurai, Arun ^a   Van Tassell, Benjamin W ^a   Yin, Chang ^a   Ockaili, Ramzi A ^a   Vigneshwar, Navin ^a   Mukhopadhyay, Nitai D ^a   Kukreja, Rakesh C ^a   Abbate, Antonio ^a   Salloum, Fadi N ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Hydrogen sulfide; Inflammasomes; MicroRNAs; Myocardial infarction

Indexed keywords

HYDROGEN SULFIDE; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MICRORNA 21; SCAFFOLD PROTEIN; SODIUM SULFIDE; ZYMOSAN; MICRORNA; MIRN21 MICRORNA, MOUSE; SULFIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CORONARY REPERFUSION; ENZYME ACTIVATION; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; INFLAMMATION; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; UPREGULATION;

ANIMALS; CELLS, CULTURED; HUMANS; HYDROGEN SULFIDE; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; SULFIDES; UP-REGULATION;

EID: 84903638746     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.113.000381     Document Type: Article

References (53)

1. Frangogiannis NG. Regulation of the inflammatory response in cardiac repair. Circ Res. 2012;110:159-173.
2. Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G. The inflammasome: a caspase-1-Activation platform that regulates immune responses and disease pathogenesis. Nat Immunol. 2009;10:241-247.
3. Mezzaroma E, Toldo S, Farkas D, Seropian IM, Van Tassell BW, Salloum FN, et al. The inflammasome promotes adverse cardiac remodeling following acute myocardial infarction in the mouse. Proc Natl Acad Sci U S A. 2011;108:19725-19730.
4. Merkle S, Frantz S, Schön MP, Bauersachs J, Buitrago M, Frost RJ, et al. A role for caspase-1 in heart failure. Circ Res. 2007;100:645-653.
5. Sandanger Ø, Ranheim T, Vinge LE, Bliksøen M, Alfsnes K, Finsen AV, et al. The NLRP3 inflammasome is up-regulated in cardiac fibroblasts and mediates myocardial ischaemia-reperfusion injury. Cardiovasc Res. 2013;99:164-174.
6. Kawaguchi M, Takahashi M, Hata T, Kashima Y, Usui F, Morimoto H, et al. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation. 2011;123:594-604.
7. Frantz S, Ducharme A, Sawyer D, Rohde LE, Kobzik L, Fukazawa R, et al. Targeted deletion of caspase-1 reduces early mortality and left ventricular dilatation following myocardial infarction. J Mol Cell Cardiol. 2003;35:685-694.
8. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, et al. H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gammalyase. Science. 2008;322:587-590.
9. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci U S A. 2007;104:15560-15565.
10. Calvert JW, Elston M, Nicholson CK, Gundewar S, Jha S, Elrod JW, et al. Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemiainduced heart failure in mice. Circulation. 2010;122:11-19.
11. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, et al. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res. 2009;105:365-374.
12. Polhemus D, Kondo K, Bhushan S, Bir SC, Kevil CG, Murohara T, et al. Hydrogen sulfide attenuates cardiac dysfunction following heart failure via induction of angiogenesis. Circ Heart Fail. 2013;6:1077-1086.
13. Su YW, Liang C, Jin HF, Tang XY, Han W, Chai LJ, et al. Hydrogen sulfide regulates cardiac function and structure in adriamycin-induced cardiomyopathy. Circ J. 2009;73:741-749.
14. Wang XH, Wang F, You SJ, Cao YJ, Cao LD, Han Q, et al. Dysregulation of cystathionine γ-lyase (CSE)/hydrogen sulfide pathway contributes to ox-LDL-induced inflammation in macrophage. Cell Signal. 2013;25:2255-2262.
15. Ganster F, Burban M, de la Bourdonnaye M, Fizanne L, Douay O, Loufrani L, et al. Effects of hydrogen sulfide on hemodynamics, inflammatory response and oxidative stress during resuscitated hemorrhagic shock in rats. Crit Care. 2010;14:R165.
16. Webb GD, Lim LH, Oh VM, Yeo SB, Cheong YP, Ali MY, et al. Contractile and vasorelaxant effects of hydrogen sulfide and its biosynthesis in the human internal mammary artery. J Pharmacol Exp Ther. 2008;324:876-882.
17. Ali MY, Ping CY, Mok YY, Ling L, Whiteman M, Bhatia M, et al. Regulation of vascular nitric oxide in vitro and in vivo; a new role for endogenous hydrogen sulphide? Br J Pharmacol. 2006;149:625-634.
18. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, et al. Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A. 2007;104:17977-17982.
19. Ali MY, Whiteman M, Low CM, Moore PK. Hydrogen sulphide reduces insulin secretion from HIT-T15 cells by a KATP channel-dependent pathway. J Endocrinol. 2007;195:105-112.
20. Salloum FN, Chau VQ, Hoke NN, Abbate A, Varma A, Ockaili RA, et al. Phosphodiesterase-5 inhibitor, tadalafil, protects against myocardial ischemia/reperfusion through protein-kinase g-dependent generation of hydrogen sulfide. Circulation. 2009;120(11 suppl):S31-S36.
21. Salloum FN, Das A, Samidurai A, Hoke NN, Chau VQ, Ockaili RA, et al. Cinaciguat, a novel activator of soluble guanylate cyclase, protects against ischemia/reperfusion injury: role of hydrogen sulfide. Am J Physiol Heart Circ Physiol. 2012;302:H1347-H1354.
22. Ji Y, Pang QF, Xu G, Wang L, Wang JK, Zeng YM. Exogenous hydrogen sulfide postconditioning protects isolated rat hearts against ischemia-reperfusion injury. Eur J Pharmacol. 2008;587:1-7.
23. Pan TT, Neo KL, Hu LF, Yong QC, Bian JS. H2S preconditioning-induced PKC activation regulates intracellular calcium handling in rat cardiomyocytes. Am J Physiol Cell Physiol. 2008;294:C169-C177.
24. Mocanu MM, Bell RM, Yellon DM. PI3 kinase and not p42/p44 appears to be implicated in the protection conferred by ischemic preconditioning. J Mol Cell Cardiol. 2002;34:661-668.
25. Tong H, Chen W, Steenbergen C, Murphy E. Ischemic preconditioning activates phosphatidylinositol-3-kinase upstream of protein kinase C. Circ Res. 2000;87:309-315.
26. Cheng Y, Zhu P, Yang J, Liu X, Dong S, Wang X, et al. Ischaemic preconditioning-regulated miR-21 protects heart against ischaemia/reperfusion injury via anti-Apoptosis through its target PDCD4. Cardiovasc Res. 2010;87:431-439.
27. Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, et al. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem. 2009;284:29514-29525.
28. Yin C, Salloum FN, Kukreja RC. A novel role of microRNA in late preconditioning: upregulation of eNOS and HSP70. Circ Res. 2009;104:572-575.
29. Kukreja RC, Yin C, Salloum FN. MicroRNAs: new players in cardiac injury and protection. Mol Pharmacol. 2011;80:558-564.
30. Sayed D, He M, Hong C, Gao S, Rane S, Yang Z, et al. MicroRNA-21 is a downstream effector of AKT that mediates its antiapoptotic effects via suppression of Fas ligand. J Biol Chem. 2010;285:20281-20290.
31. Faller S, Zimmermann KK, Strosing KM, Engelstaedter H, Buerkle H, Schmidt R, et al. Inhaled hydrogen sulfide protects against lipopolysaccharide-induced acute lung injury in mice. Med Gas Res. 2012;2:26.
32. Fox B, Schantz JT, Haigh R, Wood ME, Moore PK, Viner N, et al. Inducible hydrogen sulfide synthesis in chondrocytes and mesenchymal progenitor cells: is H2S a novel cytoprotective mediator in the inflamed joint? J Cell Mol Med. 2012;16:896-910.
33. Case SR, Martin RJ, Jiang D, Minor MN, Chu HW. MicroRNA-21 inhibits toll-like receptor 2 agonist-induced lung inflammation in mice. Exp Lung Res. 2011;37:500-508.
34. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary JJ, Ruan Q, et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol. 2010;11:141-147.
35. Chen Y, Chen J, Wang H, Shi J, Wu K, Liu S, et al. HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog. 2013;9:e1003248.
36. Das A, Smolenski A, Lohmann SM, Kukreja RC. Cyclic GMPdependent protein kinase Ialpha attenuates necrosis and apoptosis following ischemia/reoxygenation in adult cardiomyocyte. J Biol Chem. 2006;281:38644-38652.
37. Salloum FN, Abbate A, Das A, Houser JE, Mudrick CA, Qureshi IZ, et al. Sildenafil (Viagra) attenuates ischemic cardiomyopathy and improves left ventricular function in mice. Am J Physiol Heart Circ Physiol. 2008;294:H1398-H1406. (Pubitemid 351468739
38. Lamkanfi M, Malireddi RK, Kanneganti TD. Fungal zymosan and mannan activate the cryopyrin inflammasome. J Biol Chem. 2009;284:20574-20581.
39. Lamkanfi M, Mueller JL, Vitari AC, Misaghi S, Fedorova A, Deshayes K, et al. Glyburide inhibits the cryopyrin/Nalp3 inflammasome. J Cell Biol. 2009;187:61-70.
40. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16:1066-1071.
41. Johansen D, Ytrehus K, Baxter GF. Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury-Evidence for a role of K ATP channels. Basic Res Cardiol. 2006;101:53-60.
42. Mathai JC, Missner A, Kügler P, Saparov SM, Zeidel ML, Lee JK, et al. No facilitator required for membrane transport of hydrogen sulfide. Proc Natl Acad Sci U S A. 2009;106:16633-16638.
43. Hu LF, Wong PT, Moore PK, Bian JS. Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogenactivated protein kinase in microglia. J Neurochem. 2007;100:1121-1128.
44. Yang G, Pei Y, Cao Q, Wang R. MicroRNA-21 represses human cystathionine gamma-lyase expression by targeting at specificity protein-1 in smooth muscle cells. J Cell Physiol. 2012;227:3192-3200.
45. Abbate A, Van Tassell BW, Biondi-Zoccai GG. Blocking interleukin-1 as a novel therapeutic strategy for secondary prevention of cardiovascular events. BioDrugs. 2012;26:217-233.
46. Toldo S, Mezzaroma E, Abbate A. Interleukin-1 blockade in acute myocardial infarction and heart failure: ready for clinical translation Transl Med. 2012;3:e114.
47. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature. 2012;481:278-286.
48. Stutz A, Golenbock DT, Latz E. Inflammasomes: too big to miss. J Clin Invest. 2009;119:3502-3511.
49. Nicholson CK, Lambert JP, Molkentin JD, Sadoshima J, Calvert JW. Thioredoxin 1 is essential for sodium sulfide-mediated cardioprotection in the setting of heart failure. Arterioscler Thromb Vasc Biol. 2013;33:744-751.
50. Givvimani S, Munjal C, Gargoum R, Sen U, Tyagi N, Vacek JC, et al. Hydrogen sulfide mitigates transition from compensatory hypertrophy to heart failure. J Appl Physiol (1985). 2011;110:1093-1100.
51. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature. 2008;456:980-984.
52. Patrick DM, Montgomery RL, Qi X, Obad S, Kauppinen S, Hill JA, et al. Stress-dependent cardiac remodeling occurs in the absence of microRNA-21 in mice. J Clin Invest. 2010;120:3912-3916.
53. Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, Patel K, et al. Treatment of HCV infection by targeting microRNA. N Engl J Med. 2013;368:1685-1694.